Identification of regulatory and cargo proteins of endosomal and secretory pathways in arabidopsis thaliana by proteomic dissection

Molecular and Cellular Proteomics

Volumn 14, Issue 7, 2015, Pages 1796-1813

  Heard, William ^a   Sklenář, Jan ^a   Tomé, Daniel F A ^b   Robatzek, Silke ^a   Jones, Alexandra M E ^a,b  

^a SAINSBURY LABORATORY   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CESA PROTEIN; CLATHRIN LIGHT CHAIN 2; GOLGI TRANSPORT 1; GUANOSINE TRIPHOSPHATASE; PEN3 PROTEIN; PIN3 PROTEIN; PROTEOME; SNARE PROTEIN; SYNAPTOBREVIN 711; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ARABIDOPSIS PROTEIN; GREEN FLUORESCENT PROTEIN;

ARABIDOPSIS THALIANA; ARTICLE; CELL MIGRATION; CELLULAR DISTRIBUTION; CLINICAL PROTOCOL; COMPLEX FORMATION; CONTROLLED STUDY; ENDOSOME; GOLGI COMPLEX; MULTIVESICULAR BODY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEOMICS; PURIFICATION; SACCHAROMYCES; SECRETORY PATHWAY; SECRETORY VESICLE; SEEDLING; TONOPLAST; TRANS GOLGI NETWORK; AFFINITY CHROMATOGRAPHY; ARABIDOPSIS; CELL FRACTIONATION; ENDOCYTOSIS; METABOLISM; PROCEDURES; SACCHAROMYCES CEREVISIAE;

ARABIDOPSIS THALIANA;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATOGRAPHY, AFFINITY; ENDOCYTOSIS; ENDOSOMES; GREEN FLUORESCENT PROTEINS; PROTEOME; PROTEOMICS; SACCHAROMYCES CEREVISIAE; SECRETORY PATHWAY; SUBCELLULAR FRACTIONS; TRANS-GOLGI NETWORK;

EID: 84936805568     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M115.050286     Document Type: Article

References (118)

1. Park, M., and Jurgens, G., (2012) Membrane traffic and fusion at post- Golgi compartments. Front Plant Sci. 2, 111.
2. Drakakaki, G., and Dandekar, A., (2013) Protein secretion: How many secretory routes does a plant cell have? Plant Sci. 203-204, 74-78.
3. Denecke, J., Goldman, M. H., Demolder, J., Seurinck, J., and Botterman, J., (1991) The tobacco luminal binding protein is encoded by a multigene family. Plant Cell 3, 1025-1035.
4. Batoko, H., Zheng, H.-Q., Hawes, C., and Moore, I., (2000) A Rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. The Plant Cell 12, 2201-2217.
5. Reyes, F. C., Buono, R., and Otegui, M. S., (2011) Plant endosomal trafficking pathways. Curr. Opin. Plant Biol. 14, 666-673.
6. Fujimoto, M., and Ueda, T., (2012) Conserved and plant-unique mechanisms regulating plant post-Golgi traffic. Frontiers Plant Sci. 33 (197).
7. Löfke, C., Zwiewka, M., Heilmann, I., Van Montagu, M. C. E., Teichmann, T., and Friml, J., (2013) Asymmetric gibberellin signaling regulates vacuolar trafficking of PIN auxin transporters during root gravitropism. Proc. Natl. Acad. Sci. U.S.A. 110, 3627-3632.
8. Chow, C.-M., Neto, H., Foucart, C., and Moore, I., (2008) Rab-A2 and Rab-A3 GTPases Define a trans-Golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate. The Plant Cell 20, 101-123.
9. Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y.-D., and Schumacher, K., (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18, 715-730.
10. Van Damme, D., Gadeyne, A., Vanstraelen, M., Inzé, D., Van Montagu, M. C., De Jaeger, G., Russinova, E., and Geelen, D., (2011) Adaptin-like protein TPLATE and clathrin recruitment during plant somatic cytokinesis occurs via two distinct pathways. Proc. Natl. Acad. Sci. U.S.A. 108, 615-620.
11. Park, E., Diaz-Moreno, S. M., Davis, D. J., Wilkop, T. E., Bulone, V., and Drakakaki, G., (2014) Endosidin 7 specifically arrests late cytokinesis and inhibits callose biosynthesis revealing distinct trafficking events during cell plate maturation. Plant Physiol 165(3), 1019-1034.
12. Kwon, C., Bednarek, P., and Schulze-Lefert, P., (2008) Secretory pathways in plant immune responses. Plant Physiol. 147, 1575-1583.
13. Inada, N., and Ueda, T., (2014) Membrane trafficking pathways and their roles in plant-microbe interactions. Plant Cell Physiol. 55, 672-686.
14. Takano, J., Tanaka, M., Toyoda, A., Miwa, K., Kasai, K., Fuji, K., Onouchi, H., Naito, S., and Fujiwara, T., (2010) Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc. Natl. Acad. Sci. U.S.A. 107, 5220-5225.
15. Takano, J., Miwa, K., Yuan, L., von Wirén, N., and Fujiwara, T., (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc. Natl. Acad. Sci. U.S.A. 102, 12276-12281.
16. Beck, M., Zhou, J., Faulkner, C., MacLean, D., and Robatzek, S., (2012) Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. Plant Cell 24, 4205-4219.
17. Russinova, E., Borst, J. W., Kwaaitaal, M., Caño-Delgado, A., Yin, Y. H., Chory, J., and de Vries, S. C., (2004) Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16, 3216-3229.
18. Geldner, N., Hyman, D. L., Wang, X., Schumacher, K., and Chory, J., (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Development 21, 1598-1602.
19. Spallek, T., Beck, M., Ben Khaled, S., Salomon, S., Bourdais, G., Schellmann, S., and Robatzek, S., (2013) ESCRT-I mediates FLS2 endosomal sorting and plant immunity. PLoS Genet 9, e1004035.
20. Viotti, C., Bubeck, J., Stierhof, Y. D., Krebs, M., Langhans, M., van den Berg, W., van Dongen, W., Richter, S., Geldner, N., Takano, J., Jürgens, G., de Vries, S. C., Robinson, D. G., and Schumacher, K., (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22, 1344-1357.
21. Kleine-Vehn, J., Huang, F., Naramoto, S., Zhang, J., Michniewicz, M., Offringa, R., and Friml, J., (2009) PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 21, 3839-3849.
22. Bassham, D. C., Brandizzi, F., Otegui, M. S., and Sanderfoot, A. A., (2008) The secretory system of Arabidopsis. Arabidopsis Book 6, e0116.
23. Contento, A. L., and Bassham, D. C., (2012) Structure and function of endosomes in plant cells. J. Cell Sci. 125, 3511-3518.
24. Rutherford, S., and Moore, I., (2002) The Arabidopsis Rab GTPase family: Another enigma variation. Curr. Opin. Plant Biol. 5, 518-528.
25. Ueda, T., Uemura, T., Sato, M. H., and Nakano, A., (2004) Functional differentiation of endosomes in Arabidopsis cells. Plant J. 40, 783-789.
26. Geldner, N., Dénervaud-Tendon, V., Hyman, D. L., Mayer, U., Stierhof, Y.-D., and Chory, J., (2009) Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J. 59, 169-178.
27. Lu, Y. J., Schornack, S., Spallek, T., Geldner, N., Chory, J., Schellmann, S., Schumacher, K., Kamoun, S., and Robatzek, S., (2012) Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cell Microbiol. 14, 682-697.
28. Pinheiro, H., Samalova, M., Geldner, N., Chory, J., Martinez, A., and Moore, I., (2009) Genetic evidence that the higher plant Rab-D1 and Rab-D2 GTPases exhibit distinct but overlapping interactions in the early secretory pathway. J. Cell Sci. 122, 3749-3758.
29. Ueda, T., Yamaguchi, M., Uchimiya, H., and Nakano, A., (2001) Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO J. 20, 4730-4741.
30. Bottanelli, F., Gershlick, D. C., and Denecke, J., (2012) Evidence for sequential action of Rab5 and Rab7 GTPases in prevacuolar organelle partitioning. Traffic 13, 338-354.
31. Carter, C., Pan, S., Zouhar, J., Avila, E. L., Girke, T., and Raikhel, N. V., (2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. The Plant Cell 16, 3285-3303.
32. Kleffmann, T., Russenberger, D., von Zychlinski, A., Christopher, W., Sjölander, K., Gruissem, W., and Baginsky, S., (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Current Biology 14, 354-362.
33. Dunkley, T. P., Hester, S., Shadforth, I. P., Runions, J., Weimar, T., Hanton, S. L., Griffin, J. L., Bessant, C., Brandizzi, F., Hawes, C., Watson, R. B., Dupree, P., and Lilley, K. S., (2006) Mapping the Arabidopsis organelle proteome. Proc. Natl. Acad. Sci. U.S.A. 103, 6518-6523.
34. Eubel, H., Meyer, E. H., Taylor, N. L., Bussell, J. D., O'Toole, N., Heazlewood, J. L., Castleden, I., Small, I. D., Smith, S. M., and Millar, A. H., (2008) Novel proteins, putative membrane transporters, and an integrated metabolic network are revealed by quantitative proteomic analysis of Arabidopsis cell culture peroxisomes. Plant Physiol. 148, 1809-1829.
35. Jaquinod, M., Villiers, F., Kieffer-Jaquinod, S., Hugouvieux, V., Bruley, C., Garin, J., and Bourguignon, J., (2007) A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol. Cell. Proteomics 6, 394-412.
36. Schmidt, U. G., Endler, A., Schelbert, S., Brunner, A., Schnell, M., Neuhaus, H. E., Marty-Mazars, D., Marty, F., Baginsky, S., and Martinoia, E., (2007) Novel tonoplast transporters identified using a proteomic approach with vacuoles isolated from cauliflower buds. Plant Physiol. 145, 216-229.
37. Parsons, H. T., Christiansen, K., Knierim, B., Carroll, A., Ito, J., Batth, T. S., Smith-Moritz, A. M., Morrison, S., McInerney, P., Hadi, M. Z., Auer, M., Mukhopadhyay, A., Petzold, C. J., Scheller, H. V., Loqué, D., and Heazlewood, J. L., (2012) Isolation and proteomic characterization of the Arabidopsis Golgi defines functional and novel components involved in plant cell wall biosynthesis. Plant Physiol. 159, 12-26.
38. Elmore, J. M., Liu, J., Smith, B., Phinney, B., and Coaker, G., (2012) Quantitative proteomics reveals dynamic changes in the plasma membrane during Arabidopsis immune signaling. Mol. Cell. Proteomics 11, M111.014555.
39. Nikolovski, N., Rubtsov, D., Segura, M. P., Miles, G. P., Stevens, T. J., Dunkley, T. P., Munro, S., Lilley, K. S., and Dupree, P., (2012) Putative glycosyltransferases and other plant Golgi apparatus proteins are revealed by LOPIT proteomics. Plant Physiol. 160, 1037-1051.
40. Eubel, H., Heazlewood, J., and Millar, A. H. (2007) Isolation and subfractionation of plant mitochondria for proteomic analysis, in Plant Proteomics, H. Thiellement, et al., eds. Humana Press. p. 49-62.
41. Ito, J., Batth, T. S., Petzold, C. J., Redding-Johanson, A. M., Mukhopadhyay, A., Verboom, R., Meyer, E. H., Millar, A. H., and Heazlewood, J. L., (2011) Analysis of the Arabidopsis cytosolic proteome highlights subcellular partitioning of central plant metabolism. J. Proteome Res. 10, 1571-1582.
42. Morciano, M., Burré, J., Corvey, C., Karas, M., Zimmermann, H., and Volknandt, W., (2005) Immunoisolation of two synaptic vesicle pools from synaptosomes: A proteomics analysis. J. Neurochem. 95, 1732-1745.
43. Steuble, M., Gerrits, B., Ludwig, A., Mateos, J. M., Diep, T.-M., Tagaya, M., Stephan, A., Schätzle, P., Kunz, B., Streit, P., and Sonderegger, P., (2010) Molecular characterization of a trafficking organelle: Dissecting the axonal paths of calsyntenin-1 transport vesicles. Proteomics 10, 3775-3788.
44. Drakakaki, G., van de Ven, W., Pan, S., Miao, Y., Wang, J., Keinath, N. F., Weatherly, B., Jiang, L., Schumacher, K., Hicks, G., and Raikhel, N., (2012) Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res. 22, 413-424.
45. Groen, A. J., Sancho-Andrés, G., Breckels, L. M., Gatto, L., Aniento, F., and Lilley, K. S., (2014) Identification of trans-Golgi network proteins in Arabidopsis thaliana root tissue. J Proteome Res. 13, 763-776.
46. Lee, G.-J., Sohn, E. J., Lee, M. H., and Hwang, I., (2004) The Arabidopsis Rab5 homologs Rha1 and Ara7 localize to the prevacuolar compartment. Plant Cell Physiol. 45, 1211-1220.
47. Chen, X., Irani, N. G., and Friml, J., (2011) Clathrin-mediated endocytosis: The gateway into plant cells. Curr. Opin. Plant Biol. 14, 674-682.
48. Searle, B. C., (2010) Scaffold: A bioinformatic tool for validating MS/MSbased proteomic studies. Proteomics 10, 1265-1269.
49. Teo, G., Liu, G., Zhang, J., Nesvizhskii, A. I., Gingras, A. C., and Choi, H., (2014) SAINTexpress: Improvements and additional features in significance analysis of interactome software. J. Proteomics 100 37-43.
50. Choi, H., Larsen, B., Lin, Z. Y., Breitkreutz, A., Mellacheruvu, D., Fermin, D., Qin, Z. S., Tyers, M., Gingras, A. C., and Nesvizhskii, A. I., (2011) SAINT: Probabilistic scoring of affinity purification-mass spectrometry data. Nat. Methods 8, 70-73.
51. Poultney, C. S., Gutiérrez, R. A., Katari, M. S., Gifford, M. L., Paley, W. B., Coruzzi, G. M., and Shasha, D. E., (2007) Sungear: Interactive visualization and functional analysis of genomic datasets. Bioinformatics 23, 259-261.
52. Hemsley, P. A., Weimar, T., Lilley, K. S., Dupree, P., and Grierson, C. S., (2013) A proteomic approach identifies many novel palmitoylated proteins in Arabidopsis. New Phytologist 197, 805-814.
53. Sadowski, P. G., Groen, A. J., Dupree, P., and Lilley, K. S., (2008) Subcellular localization of membrane proteins. Proteomics 8, 3991-4011.
54. Parsons, H. T., Drakakaki, G., and Heazlewood, J. L., (2012) Proteomic dissection of the Arabidopsis Golgi and trans-Golgi network. Front Plant Sci. 3, 298.
55. Grefen, C., Donald, N., Hashimoto, K., Kudla, J., Schumacher, K., and Blatt, M. R., (2010) A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J. 64, 355-365.
56. Gadeyne, A., Sánchez-Rodríguez, C., Vanneste, S., Di Rubbo, S., Zauber, H., Vanneste, K., Van Leene, J., De Winne, N., Eeckhout, D., Persiau, G., Van De Slijke, E., Cannoot, B., Vercruysse, L., Mayers, Jonathan R., Adamowski, M., Kania, U., Ehrlich, M., Schweighofer, A., Ketelaar, T., Maere, S., Bednarek, Sebastian Y., Friml, J., Gevaert, K., Witters, E., Russinova, E., Persson, S., De Jaeger, G., and Van Damme, D., (2014) The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants. Cell 156, 691-704.
57. Lewis, J. D., and Lazarowitz, S. G., (2010) Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc. Natl. Acad. Sci. U.S.A. 107, 2491-2496.
58. Yamazaki, T., Kawamura, Y., Minami, A., and Uemura, M., (2008) Calcium- dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20, 3389-3404.
59. Schapire, A. L., Voigt, B., Jasik, J., Rosado, A., Lopez-Cobollo, R., Menzel, D., Salinas, J., Mancuso, S., Valpuesta, V., Baluska, F., and Botella, M. A., (2008) Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20, 3374-3388.
60. Zhang, H., Zhang, L., Gao, B., Fan, H., Jin, J., Botella, M. A., Jiang, L., and Lin, J., (2011) Golgi apparatus-localized synaptotagmin 2 is required for unconventional secretion in Arabidopsis. PLoS One 6, e26477.
61. Conchon, S., Cao, X., Barlowe, C., and Pelham, H. R., (1999) Got1p and Sft2p: Membrane proteins involved in traffic to the Golgi complex. EMBO J. 18, 3934-3946.
62. Oikawa, A., Lund, C. H., Sakuragi, Y., and Scheller, H. V., (2013) Golgilocalized enzyme complexes for plant cell wall biosynthesis. Trends Plant Sci. 18, 49-58.
63. Waugh, M. G., Chu, K. M., Clayton, E. L., Minogue, S., and Hsuan, J. J., (2011) Detergent-free isolation and characterization of cholesterol-rich membrane domains from trans-Golgi network vesicles. J. Lipid Res. 52, 582-589.
64. Weinberger, A., (2005) Control of Golgi morphology and function by Sed5 t-SNARE phosphorylation. 16(10), 4918-4930.
65. Uemura, T., Ueda, T., Ohniwa, R. L., Nakano, A., Takeyasu, K., and Sato, M. H., (2004) Systematic analysis of SNARE molecules in Arabidopsis: Dissection of the post-Golgi network in plant cells. Cell Structure Function 29, 49-65.
66. Brandizzi, F., and Barlowe, C., (2013) Organization of the ER-Golgi interface for membrane traffic control. Nat. Rev. Mol. Cell Biol. 14, 382-392.
67. Boevink, P., Oparka, K., Santa Cruz, S., Martin, B., Betteridge, A., and Hawes, C., (1998) Stacks on tracks: The plant Golgi apparatus traffics on an actin/ER network. Plant J. 15, 441-447.
68. Stefano, G., Hawes, C., and Brandizzi, F., (2014) ER-The key to the highway. Curr. Opin. Plant Biol. 22, 30-38.
69. Sparkes, I. A., Frigerio, L., Tolley, N., and Hawes, C., (2009) The plant endoplasmic reticulum: A cell-wide web. Biochem. J. 423, 145-155.
70. Lorente-Rodríguez, A., Heidtman, M., and Barlowe, C., (2009) Multicopy suppressor analysis of thermosensitive YIP1 alleles implicates GOT1 in transport from the ER. J. Cell Sci. 122, 1540-1550.
71. Chen, J., Stefano, G., Brandizzi, F., and Zheng, H., (2011) Arabidopsis RHD3 mediates the generation of the tubular ER network and is required for Golgi distribution and motility in plant cells. J. Cell Sci. 124, 2241-2252.
72. Saito, C., and Ueda, T., (2009) Chapter 4 Functions of RAB and SNARE Proteins in Plant Life, in International Review of Cell and Molecular Biology, W. J. Kwang, ed. Academic Press. p. 183-233.
73. Ueda, T., Matsuda, N., Anai, T., Tsukaya, H., Uchimiya, H., and Nakano, A., (1996) An Arabidopsis gene isolated by a novel method for detecting genetic interaction in yeast encodes the GDP dissociation inhibitor of Ara4 GTPase. Plant Cell 8, 2079-2091.
74. Zarský, V., Cvrcková, F., Bischoff, F., and Palme, K., (1997) At-GDI1 from Arabidopsis thaliana encodes a rab-specific GDP dissociation inhibitor that complements the sec19 mutation of Saccharomyces cerevisiae. FEBS Lett. 403, 303-308.
75. Sivars, U., Aivazian, D., and Pfeffer, S. R., (2003) Yip3 catalyses the dissociation of endosomal Rab-GDI complexes. Nature 425, 856-859.
76. Chen, C. Z., and Collins, R. N., (2005) Insights into biological functions across species: Examining the role of Rab proteins in YIP1 family function. Biochem. Soc. Trans. 33, 614-618.
77. Kano, F., Yamauchi, S., Yoshida, Y., Watanabe-Takahashi, M., Nishikawa, K., Nakamura, N., and Murata, M., (2009) Yip1A regulates the COPIindependent retrograde transport from the Golgi complex to the ER. J. Cell Sci. 122, 2218-2227.
78. Alvim Kamei, C. L., Boruc, J., Vandepoele, K., Van den Daele, H., Maes, S., Russinova, E., Inzé, D., and De Veylder, L., (2008) The PRA1 gene family in Arabidopsis. Plant Physiol. 147, 1735-1749.
79. Gendre, D., McFarlane, H. E., Johnson, E., Mouille, G., Sjödin, A., Oh, J., Levesque-Tremblay, G., Watanabe, Y., Samuels, L., and Bhalerao, R. P., (2013) Trans-Golgi network localized ECHIDNA/Ypt interacting protein complex is required for the secretion of cell wall polysaccharides in Arabidopsis. Plant Cell 25, 2633-2646.
80. Goh, T., Uchida, W., Arakawa, S., Ito, E., Dainobu, T., Ebine, K., Takeuchi, M., Sato, K., Ueda, T., and Nakano, A., (2007) VPS9a, the common activator for two distinct types of Rab5 GTPases, is essential for the development of Arabidopsis thaliana. The Plant Cell 19, 3504-3515.
81. Uejima, T., Ihara, K., Goh, T., Ito, E., Sunada, M., Ueda, T., Nakano, A., and Wakatsuki, S., (2010) GDP-bound and nucleotide-free intermediates of the guanine nucleotide exchange in the Rab5.Vps9 system. J. Biol. Chem. 285, 36689-36697.
82. Thellmann, M., Rybak, K., Thiele, K., Wanner, G., and Assaad, F. F., (2010) Tethering factors required for cytokinesis in Arabidopsis. Plant Physiol. 154, 720-732.
83. Wang, W., Sacher, M., and Ferro-Novick, S., (2000) TRAPP stimulates guanine nucleotide exchange on Ypt1p. J. Cell Biol. 151, 289-296.
84. Sacher, M., Kim, Y. G., Lavie, A., Oh, B. H., and Segev, N., (2008) The TRAPP complex: Insights into its architecture and function. Traffic 9, 2032-2042.
85. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A., and Jürgens, G., (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219-230.
86. Naramoto, S., Otegui, M. S., Kutsuna, N., de Rycke, R., Dainobu, T., Karampelias, M., Fujimoto, M., Feraru, E., Miki, D., Fukuda, H., Nakano, A., and Friml, J., (2014) Insights into the localization and function of the membrane trafficking regulator GNOM ARF-GEF at the Golgi apparatus in Arabidopsis. Plant Cell 26, 3062-3076.
87. Uemura, T., and Ueda, T., (2014) Plant vacuolar trafficking driven by RAB and SNARE proteins. Curr. Opin. Plant Biol. 22, 116-121.
88. Nomura, K., Debroy, S., Lee, Y.H., Pumplin, N., Jones, J., He, S.Y. (2006) A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science. Jul 14, 313, (5784), 220-223.
89. Tanaka, H., Kitakura, S., De Rycke, R., De Groodt, R., and Friml, J., (2009) Fluorescence imaging-based screen identifies ARF GEF component of early endosomal trafficking. Curr. Biol. 19, 391-397.
90. Bonifacino, J. S., and Hierro, A., (2011) Transport according to GARP: Receiving retrograde cargo at the trans-Golgi network. Trends Cell Biol. 21, 159-167.
91. Miller, V. J., Sharma, P., Kudlyk, T. A., Frost, L., Rofe, A. P., Watson, I. J., Duden, R., Lowe, M., Lupashin, V. V., and Ungar, D., (2013) Molecular insights into vesicle tethering at the Golgi by the conserved oligomeric Golgi (COG) complex and the golgin TATA element modulatory factor (TMF). J. Biol. Chem. 288, 4229-4240.
92. Hong, W., and Lev, S., (2014) Tethering the assembly of SNARE complexes. Trends Cell Biol. 24, 35-43.
93. Latijnhouwers, M., Hawes, C., and Carvalho, C., (2005) Holding it all together? Candidate proteins for the plant Golgi matrix. Curr. Opin. Plant Biol. 8, 632-639.
94. Oda, Y., Iida, Y., Nagashima, Y., Sugiyama, Y., and Fukuda, H., (2015) Novel coiled-coil proteins regulate exocyst association with cortical microtubules in xylem cells via the conserved oligomeric Golgi-complex 2 protein. Plant Cell Physiol. 56, 277-286.
95. Pahari, S., Cormark, R. D., Blackshaw, M. T., Liu, C., Erickson, J. L., and Schultz, E. A., (2014) Arabidopsis UNHINGED encodes a VPS51 homolog and reveals a role for the GARP complex in leaf shape and vein patterning. Development 141, 1894-1905.
96. Koumandou, V. L., Dacks, J. B., Coulson, R. M., and Field, M. C., (2007) Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol. Biol. 7, 29.
97. Conibear, E., Cleck, J. N., and Stevens, T. H., (2003) Vps51p mediates the association of the GARP (Vps52/53/54) complex with the late Golgi t-SNARE Tlg1p. Mol. Biol. Cell 14, 1610-1623.
98. Conibear, E., and Stevens, T. H., (2000) Vps52p, Vps53p, and Vps54p form a novel multisubunit complex required for protein sorting at the yeast late Golgi. Mol. Biol. Cell 11, 305-323.
99. Feraru, E., Feraru, M. I., Asaoka, R., Paciorek, T., De Rycke, R., Tanaka, H., Nakano, A., and Friml, J., (2012) BEX5/RabA1b Regulates trans- Golgi network-to-plasma membrane protein trafficking in Arabidopsis. The Plant Cell 24, 3074-3086.
100. Ebine, K., Fujimoto, M., Okatani, Y., Nishiyama, T., Goh, T., Ito, E., Dainobu, T., Nishitani, A., Uemura, T., Sato, M. H., Thordal-Christensen, H., Tsutsumi, N., Nakano, A., and Ueda, T., (2011) A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat. Cell Biol. 13, 853-859.
101. Schellmann, S., and Pimpl, P., (2009) Coats of endosomal protein sorting: Retromer and ESCRT. Curr. Opin. Plant Biol. 12, 670-676.
102. Jaillais, Y., Fobis-Loisy, I., Miège, C., Rollin, C., and Gaude, T., (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443, 106-109.
103. Lee, Y., Jang, M., Song, K., Kang, H., Lee, M. H., Lee, D. W., Zouhar, J., Rojo, E., Sohn, E. J., and Hwang, I., (2013) Functional identification of sorting receptors involved in trafficking of soluble lytic vacuolar proteins in vegetative cells of Arabidopsis. Plant Physiol. 161, 121-133.
104. Di Sansebastiano, G. P., (2013) Defining new SNARE functions: The i- SNARE. Front Plant Sci. 4, 99.
105. González, E., Solano, R., Rubio, V., Leyva, A., and Paz-Ares, J., (2005) Phosphate transporter traffic facilitator1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a highaffinity phosphate transporter in Arabidopsis. Plant Cell 17, 3500-3512.
106. Bahk, J. D., Bang, W. Y., and Heo, J. B., (2009) Plant PRA plays an important role in intracellular vesicular trafficking between compartments as GDF. Plant Signal. Behavior 4, 1094-1095.
107. Lee, M. H., Jung, C., Lee, J., Kim, S. Y., Lee, Y., and Hwang, I., (2011) An Arabidopsis prenylated Rab acceptor 1 isoform, AtPRA1.B6, displays differential inhibitory effects on anterograde trafficking of proteins at the endoplasmic reticulum. Plant Physiol. 157, 645-658.
108. Schumacher, K., and Krebs, M., (2010) The V-ATPase: small cargo, large effects. Curr Opin Plant Biol 13, 724-730.
109. Friml, J., Wis̈niewska, J., Benková, E., Mendgen, K., and Palme, K., (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806-809.
110. Meyer, D., Pajonk, S., Micali, C., O'Connell, R., and Schulze-Lefert, P., (2009) Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J. 57, 986-999.
111. Paredez, A. R., Somerville, C. R., and Ehrhardt, D. W., (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491-1495.
112. Sanderfoot, A. A., Assaad, F. F., and Raikhel, N. V., (2000) The Arabidopsis genome. An abundance of soluble N-ethylmaleimide-sensitive factor adaptor protein receptors. Plant Physiol. 124, 1558-1569.
113. Robinson, D. G., Herranz, M.-C., Bubeck, J., Pepperkok, R., and Ritzenthaler, C., (2007) Membrane dynamics in the early secretory pathway. Critical Reviews in Plant Sciences 26, 199-225.
114. Shahriari, M., Richter, K., Keshavaiah, C., Sabovljevic, A., Huelskamp, M., and Schellmann, S., (2011) The Arabidopsis ESCRT protein-protein interaction network. Plant Molecular Biol. 76, 85-96.
115. Zhang, Y., Liu, C.-M., Emons, A.-M. C., and Ketelaar, T., (2010) The plant exocyst. J. Integrative Plant Biol. 52, 138-146.
116. Vernoud, V., Horton, A. C., Yang, Z., and Nielsen, E., (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol. 131, 1191-1208.
117. Latijnhouwers, M., Gillespie, T., Boevink, P., Kriechbaumer, V., Hawes, C., and Carvalho, C. M., (2007) Localization and domain characterization of Arabidopsis golgin candidates. J. Experiment. Botany 58, 4373-4386.
118. Masclaux, F. G., Galaud, J. P., and Pont-Lezica, R., (2005) The riddle of the plant vacuolar sorting receptors. Protoplasma 226, 103-108.